Exploring the Arctic Charr Intestinal Glycome: Evidence of Increased N-Glycolylneuraminic Acid Levels and Changed Host–Pathogen Interactions in Response to Inflammation

Abstract

Disease outbreaks are a limiting factor for the sustainable development of the aquaculture industry. The intestinal tract is covered by a mucus layer mainly comprised by highly glycosylated proteins called mucins. Mucins regulate pathogen adhesion, growth, and virulence, and the glycans are vital for these functions. We analyzed intestinal mucin O-glycans on mucins from control and full-fat extruded soy-bean-fed (known to cause enteritis) Arctic charr using liquid chromatography–tandem mass spectrometry. In total, 56 glycans were identified on Arctic charr intestinal mucins, with a high prevalence of core-5-type and sialylated O-glycans. Disialic-acid-epitope-containing structures including NeuAcα2,8NeuAc, NeuAc­(Gc)­α2,8NeuGc­(Ac), and NeuGcα2,8NeuGc were the hallmark of Arctic charr intestinal mucin glycosylation. Arctic charr fed with soy bean meal diet had lower (i) number of structures detected, (ii) interindividual variation, and (iii) N-glycolylneuraminic-acid-containing glycans compared with control Arctic charr. Furthermore, Aeromonas salmonicida grew less in response to mucins from inflamed Arctic charr than from the control group. The Arctic charr glycan repertoire differed from that of Atlantic salmon. In conclusion, the loss of N-glycolylneuraminic acid may be a biomarker for inflammation in Arctic char, and inflammation-induced glycosylation changes affect host–pathogen interactions.

Effects of Size and Geographical Origin on Atlantic salmon, Salmo salar, Mucin O-Glycan Repertoire

“…Currently, it is not known whether this situation is general for Atlantic salmon or population-specific for a single geographical location. Decreased interindividual variation in response to inflammation has been demonstrated among mucin O -glycans from Artic charr ( Salvelinus alpinus ) (14).…”

Stress Impairs Skin Barrier Function and Induces α2-3 Linked N-Acetylneuraminic Acid and Core 1 O-Glycans on Skin Mucins in Atlantic Salmon, Salmo salar

“…The related species Arctic charr (Salvelinus alpinus) displays increased levels of NeuGc in response to inflammation in the gastrointestinal tract mucins [22]. Here, we found a trend towards increased NeuGc O-glycan structures on Atlantic salmon skin mucins from stressed fish, suggesting that an increase in NeuGc O-glycan structures may be associated with a broad range of stressors.…”

“…Mucin glycosylation can govern bacterial adhesion, virulence and growth [22,25,26,30,31,[50][51][52], and glycosylation changes modulate host-bacterial interactions [23,25]. Consequently, the stress-induced glycosylation changes have the potential to affect the sensitivity towards infection, as well as the normal microbiota.…”

“…Mucins are highly glycosylated and 50-90% of their total weight might be composed of carbohydrates [20]. The mucin glycans can be very diverse, and change in response to environmental factors [21], which has been demonstrated, e.g., during soy-bean-induced enteritis in arctic char (Salvelinus alpinus) [22], and in mammals during infections [23][24][25]. These changes in glycosylation, governed by glycosyltransferases and substrate availability, in turn affect the interactions between host and pathogen [24][25][26].…”

Genomics of host-pathogen interactions: challenges and opportunities across ecological and spatiotemporal scales

“…Interactions between host glycans and pathogens are thus central for host-pathogen specificity and virulence. As such, one would expect that host glycans and pathogen adhesins are subjected to strong selective pressure (Linden et al., 2008a; Lindén et al., 2008b; Linden et al., 2010, 2010; Vitiazeva et al, 2015; Venkatakrishnan et al, 2017; Venkatakrishnan et al, 2019). While certain individual interactions between host glycans and pathogen adhesins have been dissected in detail (Rydell et al, 2011; Bugaytsova et al, 2017) it remains difficult to actually identify different glycoconjugate compositions and their underlying genetic basis.While enzymes involved in glycan biosynthesis are easily identified based on sequence identity (curated collection: http://www.cazy.org; Lombard et al, 2013) and make up about 5% of the total genome (Rini, Varki & Esko, 2015) the resulting glycan structures are governed by stochastic events, substrate availability and state of differentiation and physiological environment.…”